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Construction of the Auditorium was a massive undertaking, illustrating the vision of church Prophet/President Frederick M. Smith who provided the building's inspiration. Groundbreaking began in 1926 and the building was only completed in 1958. The Conference Chamber was originally supposed to be about 66% larger than it is today according to the vision of Frederick M. Smith. Construction was virtually halted during the Great Depression when the church struggled under a massive debt.

The Auditorium houses an Aeolian-Skinnerpipe organ with 113 ranks and 6,334 pipes. The Auditorium Organ includes an antiphonal console and pipes in the rear balcony of the oval chamber. It is listed as one of the top 75 largest pipe organs in the world.[1]

The Children's Peace Pavilion, located in the Auditorium, was established in 1995 to pursue its mission of "Enriching the lives of children through the pursuit of peace for all." It attracts visitors each year to a number of exhibits designed to teach concepts of personal peace, social peace, international peace, and environmental peace to children ages 5 through 11. It is frequently used as a destination for elementary school field trips for students in the greater Kansas City area. Local Girl Scouts may also earn Girl Scouts of the USA insignia through a partnership with Children's Peace Pavilion. As an independent 501(c)3 charitable organization, Children's Peace Pavilion is governed by an independent board of directors.

World Conferences of the church are traditionally held here every two years in the World Conference Chamber, a large hall which seats nearly 6,000. The Conference Chamber is 214' x 168' and it is 92' from the floor to the height of the dome's interior. The exterior of the dome is 114' above street level. Originally, the Auditorium was supposed to have two balconies but was restricted to one balcony to financial limitations. In retrospect, two balconies would have caused acoustical damage to the Auditorium.

In addition to its use by the church, the Auditorium is made available for high school graduations and cultural events in the Independence and Kansas City, Missouri area. Numerous dignitaries have spoken in the Auditorium. On June 27, 1945 Independence native Harry S. Truman spoke at the Auditorium during his first return trip to Independence during his presidency. During his remarks, which were also attended by First Lady Bess Truman and their daughter Margaret Truman, President Truman announced that the United States had become a signatory to the United Nations treaty. Former Secretary of State Colin Powell delivered an address at the Auditorium on July 24, 1998 commemorating the 50th anniversary of the executive order that led to the desegregation of the United States military. Primate researcher and environmentalist Jane Goodall spoke at the Auditorium in 1999. On July 5, 2007, former United States President Bill Clinton gave the keynote address at the Auditorium commemorating the 50th anniversary of the Truman Presidential Library.